LETTER
doi:10.1038/nature11135
Discovery of a sensory organ that coordinates lunge
feeding in rorqual whales
Nicholas D. Pyenson1,2, Jeremy A. Goldbogen3, A. Wayne Vogl4, Gabor Szathmary5, Richard L. Drake6 & Robert E. Shadwick7
Top ocean predators have evolved multiple solutions to the
challenges of feeding in the water1–3. At the largest scale, rorqual
whales (Balaenopteridae) engulf and filter prey-laden water by
lunge feeding4, a strategy that is unique among vertebrates1.
Lunge feeding is facilitated by several morphological specializations, including bilaterally separate jaws that loosely articulate
with the skull5,6, hyper-expandable throat pleats, or ventral groove
blubber7, and a rigid y-shaped fibrocartilage structure branching
from the chin into the ventral groove blubber8. The linkages and
functional coordination among these features, however, remain
poorly understood. Here we report the discovery of a sensory organ
embedded within the fibrous symphysis between the unfused jaws
that is present in several rorqual species, at both fetal and adult
stages. Vascular and nervous tissue derived from the ancestral,
anterior-most tooth socket insert into this organ, which contains
connective tissue and papillae suspended in a gel-like matrix. These
papillae show the hallmarks of a mechanoreceptor, containing
nerves and encapsulated nerve termini. Histological, anatomical
and kinematic evidence indicate that this sensory organ responds
to both the dynamic rotation of the jaws during mouth opening
and closure, and ventral groove blubber7 expansion through direct
mechanical linkage with the y-shaped fibrocartilage structure.
Along with vibrissae on the chin9, providing tactile prey sensation,
this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment,
a paradigm that is consistent with unsteady hydrodynamic
models and tag data from lunge-feeding rorquals10–13. Despite the
antiquity of unfused jaws in baleen whales since the late Oligocene14
( 23–28 million years ago), this organ represents an evolutionary
novelty for rorquals, based on its absence in all other lineages of
extant baleen whales. This innovation has a fundamental role in one
of the most extreme feeding methods in aquatic vertebrates, which
facilitated the evolution of the largest vertebrates ever.
Large marine suspension feeders have evolved many times over the
past 200 million years (Myr)1–3. These vertebrates, which include
extinct bony fish, chondrichthyans and baleen whales (Mysticeti), all
show similar morphological specializations for feeding in water while
maintaining large body sizes2,3. For those vertebrates with solely
aquatic ancestries, such as bony fish and chondrichthyans, feeding
modes mostly consist of variations on unidirectional ram filter feeding,
using gill rakers1. By contrast, baleen whales are secondarily adapted to
marine environments from a terrestrial ancestry3. Their feeding specializations thus reflect a trade-off between evolutionary innovations
(for example, baleen) and fundamental constraints from a mammalian
body plan (such as air breathing)3. The origin of suspension feeding in
mysticetes represents an evolutionary novelty with no parallel in any
other mammalian or known synapsid lineage15. Moreover, the innovation of baleen preceded the origin of extremely large body sizes in
mysticetes16, which rank among the largest vertebrates ever.
Although mysticetes use several different modes of filter feeding3,
rorquals exclusively engulf large volumes of prey-laden water in a
single, rapid gulp4. In fin whales (Balaenoptera physalus), for example,
the entire process of a lunge occurs in a short time span (,6 s), during
which approximately 60–80 m3 of water and prey are engulfed, a
volume equal to or greater than that of the individual rorqual itself17
(Fig. 1). During a lunge, rorquals accelerate to high speed and open
their jaws in a complex sequence of rotation around three orthogonal
axes6, including an overall gape angle that approaches 90 degrees at the
peak of the lunge5. Dynamic pressure imposed on the floor of the
mouth forces inversion of the tongue18 and expansion of the ventral
groove blubber (VGB) to accommodate the engulfed water5,7. Hydromechanical models suggest that the expansion of the oropharyngeal
cavity (or ventral pouch8) requires active resistance, in a highly coordinated fashion, by eccentric action from musculature associated with
the VGB10–13. The lunge sequence ends once the mandibles close
around the volume of engulfed water, with the VGB and the oropharyngeal cavity slowly returning to its original size, allowing the baleen
plates to filter the captured prey from the engulfed water3.
a
ma
me
so
Stem of YSF
b
c
Right YSF branch
1m
vib
Left
YSF branch
Figure 1 | Key jaw anatomy of a rorqual lunge, shown in a fin whale (B.
physalus). a, Jaw in oblique view. b, Laterally extensible, accordion-like VGB.
c, YSF embedded in the VGB of an adult fin whale, demarcated by arrows and
digitally enhanced with a low opacity mask. ma, mandibles; me, mental
foramina; so, sensory organ; vib, vibrissae. Art by C. Buell.
1
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, District of Columbia 20013-7013, USA. 2Departments of Mammalogy and
Paleontology, Burke Museum of Natural History and Culture, Seattle, Washington 98195, USA. 3Cascadia Research Collective, 218K West 4th Avenue, Olympia, Washington 98501, USA. 4Department of
Cellular and Physiological Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada. 5FPInnovations, 2665 East Mall, Vancouver, British Columbia V6T 1W5, Canada.
6
Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio 44195, USA. 7Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4,
Canada.
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LETTER RESEARCH
the mandibles, a structure that is homologous with the lower first
incisor tooth socket of fossil ‘toothed’ mysticetes14–16. The presence
and identity of these neurovascular bundles, which contain branches
of the mandibular division of the trigeminal nerve, were confirmed by
subsequent dissection of the same specimen. They were also present in
fetal specimens of the same species (see Supplementary Information).
Three-dimensional renderings also indicated that these bundles are
asymmetrically arranged, with a single bundle extending medially
from one mandible. We verified that this asymmetry fluctuates in
dominance, with 60% from the left in fin whales (n 5 10). In minke
whales (Balaenoptera acutorostrata), we observed bundle dominance
from both the left and right (n 5 2). XRCT and MRI scans showed the
precise anatomical geometry of the organ relative to the distal ends of
the mandibles (Fig. 3), with XRCT indicating that the organ directly
overlies the anterior termination of the YSF stem along the anterior
margin of the throat pouch. This configuration provides the mechanical linkages that connect this organ to both bony and soft tissues
(that is, the rotation of the bony mandibles6 and the expansion of the
throat pleats7) during the course of a single lunge (Fig. 1).
Following initial observations8, it was suggested that the mandibular
symphysis in fin whales contained a synovial cavity19. Our results show
that the symphysis is unlike a typical synovial joint with cartilage.
Instead, it is bridged by very dense connective tissue, with cruciate
fibres, but without true or patent ligaments that originate from the
symphyseal groove. In addition, our anatomical and histological analyses indicate that its overall geometry and specialized tissues satisfy
the criteria of a sensory organ. Specifically, we argue that the organ
responds to localized changes in jaw configuration during lunge feeding, in which the rotation of the bowed jaws will cause deformation of
the symphysis, similar to an intervertebral joint20. This action provides
the mechanical input to the sensory organ, which the brain receives
through the mandibular branch of the trigeminal nerve (Fig. 3). The
organ’s asymmetric vascularization and innervation is the first such
fluctuating asymmetry reported in the soft tissue of mysticetes,
although asymmetric morphology is not unprecedented in toothed
In addition to the accordion-like VGB, lunge feeding is facilitated by
a suite of bony and soft tissue morphological adaptations5–9 (Fig. 1).
The lower jaw consists of two mandibles unfused at the symphysis and
flexibly anchored to the skull by fibrous joints5,6. These atypical fibrous
temporomandibular joints5 increase kinetic freedom and resist shear
forces during the rapid excursions of a lunge. The mandibular symphysis has a direct mechanical linkage to the VGB7 through the
y-shaped fibrocartilage (YSF) structure8, which has a raised stem that
emerges from the symphysis and extends posteriorly in two branches,
parallel to the jaws and embedded within the VGB8. How these structures are integrated into the engulfment apparatus has remained
enigmatic, although hydro-mechanical models and kinematic data
from tagged rorquals suggest that lunge feeding is a highly coordinated
process10–13. Here, we identify a novel sensory organ that is mechanically
linked to both bony and soft tissues, and can provide the brain with
mechanosensory information for coordinating the rapid and marked
expansion of the oral cavity during a lunge.
We analysed the functional morphology of the mandibular symphysis
in small, medium and large balaenopterid species, including both adult
and fetal specimens (see Supplementary Information). Midline sagittal
cuts along the mandibular symphysis showed that the sensory organ is
mostly located on the dorsal half of the region between the symphyseal
surfaces of the mandibles, and occupies a roughly spheroidal cavity.
The organ is bound on all sides by dense connective tissue; the inner
surface of the cavity is lined by a discontinuous squamous layer of cells
and filled with a viscous gel-like matrix. The gel-like matrix supports
numerous small connective tissue papillae that extend from the inner
surface and sometimes cluster in irregular numbers within the cavity.
Notably, the papillae contain nerves and encapsulated nerve termini
(Fig. 2).
We also analysed the three-dimensional soft-tissue anatomy of an
adult fin whale mandibular symphysis before dissection, using both
magnetic resonance imaging (MRI) and X-ray computed tomography
(XRCT) scanning (Fig. 3). Our analyses showed that the organ receives
neurovascular bundles that emerge from vestigial alveolar foramina of
a
b
c
raf
d
20 μm
Nerve
e
in e
pa
ma
so
so
10 cm
f
dors
g
2 mm
150 μm
h
Branch of
inferior alveolar
artery
post
nvb
Artery
raf
Transverse
section through
right ma
10 cm
Figure 2 | Anatomy and histology of the rorqual mandibular symphysis,
shown in fin whales (B. physalus). a, b, Mandibular symphysis in sagittal
section, showing bony and soft tissue around the sensory organ (so) and
papillae (pa) within it. raf, relictual alveolar foramen. c–e, Luxol fast blue
histological stains showing neurovascular bundles (nvb) and cell layers within
Branch of
inferior alveolar 1 cm
nerve
Nerve
2 mm
the sensory organ, with arrows pointing to discontinuous squamous cell layer
in d and nerve termini in e. f, g, Dissection showing neurovascular bundles in
close association with the alveolar groove. dors, dorsal; post, posterior.
h, Histological section of the tissue shown in g. Art by C. Buell.
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RESEARCH LETTER
a
b
raf
ma
ma
so
vib
d
c
so
so
e
nvb
so
10 cm
e, f
d
so
f
vib
Stem of YSF
raf
raf
so
g
ma
dors
dors
Stem of YSF
h
Stem of YSF
i
j
raf
k
so
nvb
nvb
so nvb
j
i
h
ma
ant
dors
so
so
so
Figure 3 | Digital imaging of the rorqual chin, shown in fin whales (B.
physalus). a, Mandibular symphysis showing bony and neurovascular tissue
around the sensory organ (so). b, Three-dimensional XRCT rendering of
a, showing the mandibles (ma), sensory organ and YSF and location of slices
d–f. c, Chin of an adult fin whale. d–g, Transverse XRCT slices through the chin
(g) showing the sensory organ (light green) in different thicknesses.
h–j, Coronal MRI slices through the chin. k, Asymmetric neurovascular
bundles (nvb), with mandibles digitally removed for clarity, and location of
MRI slices j–h. Ant, anterior. Art by C. Buell.
whales, for both bony tissue (for example, tusks in narwhals (Monodon
monoceros21)) and soft tissue (for example, nasal sacs and bursae22).
The asymmetry associated with this sensory organ may reflect
lateralized feeding behaviours (for example, rolling, side gulping) that
have individual side biases for several rorqual species23,24.
The new rorqual morphology described here provides yet another
example of how aquatic25 and marine mammals26 have evolved unique
sensory systems to navigate, communicate and feed in the water27.
Mechanoreceptors embedded within fibrous mandibular symphyses
have been observed in other terrestrial mammals28, but rorquals alone
possess clear mechanoreceptors suspended within a gel-like cavity
between a completely unfused symphysis. In terms of lunge-feeding
kinematics, anatomical and histological evidence suggest that the
organ’s mechanosensors assist in controlling and providing neurological information about the configuration of the jaws during rapid
lunges. We propose a three-step lunge-feeding model to explain the
organ’s role during a lunge: (1) using vibrissae present on the external
surface of the chin9, rorquals register prey fields of sufficient density;
(2) the jaws disengage and rotate6, thereby compressing and shearing
the organ; and (3) the oropharyngeal cavity reaches full expansion,
with drag forces acting on the inside of the mouth17,18 transmitted to
the organ through the YSF8 (Fig. 2). According to dynamic modelling
studies10–13, rorquals must actively control the rate of mouth opening
and throat-pouch expansion to effectively maximize volume captured;
we propose that the sensory organ has a key role in coordinating this
movement.
The discovery of this organ raises questions about its role in the
evolution of lunge feeding in whales. The ancestral mandibular condition of modern cetaceans was probably a fused (or strong sutural)
symphysis28 with an elongate surface14, as seen in nearly all basilosaurids,
and a fused symphysis persists in modern toothed whales. By contrast,
all living mysticetes possess unfused symphyses3,14–16. Recently
described fossil evidence from Janjucetus hunderi, a stem ‘toothed’
mysticete, demonstrates that the transition from fused to unfused
mandibles occurred early in baleen whale evolution, with unfused
symphyses in mysticetes having a late Oligocene antiquity
(,23–28 Myr ago)14. Our investigations of the mandibular symphyses
in living mysticetes show that bowhead, right and pygmy right whales
(Balaena mysticetus, Eubalaena spp. and Caperea marginata, respectively) do not possess a gel-like cavity in their mandibular symphysis,
although small papillae intruding into the connective-tissue matrix in
this area are patent among adult and immature specimens (see
Supplementary Information). The condition of the mandibular symphysis in grey whales (Eschrichtius robustus) has only been reported for
a decayed neonatal specimen29, although the suggestion of a mucoid
centre is broadly similar with the morphology of the organ described
here. On the basis of this equivocal evidence, we propose that the organ
evolved either at the node of Balaenopteroidea (grey whales and
rorquals), or along the stem to crown Balaenopteridae (rorquals)15. If
the former, the organ is a pre-adaptation for lunge feeding; if the latter,
the organ evolved in tandem with VGB and specializations of the
mandible morphology, such as a laterally deflected coronoid process6
and flexible temporomandibular joints5, which exhibit a degree of
mandible rotation and oropharyngeal cavity expansion far greater than
that of grey whales29. Regardless of evolutionary sequence, we argue
that multiple lines of evidence indicate that the sensory organ has a key
role in lunge feeding by registering the rotation of the mandibles during
a lunge and the expansion of the throat pouch through the YSF, all of
which evolved before the extremely large body sizes observed in today’s
rorquals. Despite the opportunity to observe the adult morphology of
large rorquals during decades of sustained hunting30, these findings
demonstrate how poorly we understand the basic functional morphology of these ecologically important ocean predators.
METHODS SUMMARY
Fieldwork. We recorded macroscopic observations and collected tissue samples
from fresh fin whale carcasses that were collected as part of commercial catch
operations in Hvalfjörður, Iceland, in 2009 and 2010, as well as carcasses of minke
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LETTER RESEARCH
whales collected by Hrefnuveiðimenn ehf in 2010. For both species, intact
carcasses belonged to adult individuals and had been dead for less than 24 h.
We directly observed the sensory organ in all of the specimens in which we
dissected the mandibular symphysis (see Supplementary Information). All tissue
samples from Iceland were transferred and imported to Canada under Convention
on International Trade in Endangered Species of Wild Fauna and Flora (CITES)
permits.
Imaging and histology. XRCT scanning was conducted on frozen specimens of
B. physalus and B. acutorostrata at the CT Imaging Centre at the FPInnovations
Wood Products Division, using a 4 MeV linear accelerator X-ray source with
0.4 mm spatial resolution, and with a large (1 m) scanning envelope. CT images
were rendered using VGStudioMax 2.0 software. MRI scans were conducted on a
1.5 Tesla General Electric superconducting magnetic resonance system at the UBC
MRI facility. MRI volume-rendered images were produced at the Cleveland Clinic
Lerner College of Medicine of Case Western Reserve University, with a volumerendering technique using the Inspace application on a Siemens Multimodality
Work Place with VE36A software and Fijitsu hardware. Tissues were fixed in
standard buffered formalin for histology. Sections were stained using either a
generalized haematoxylin and eosin stain or a myelin stain (Luxol fast blue),
following protocols devised at Wax-it Histology Services.
Received 27 January; accepted 4 April 2012.
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Supplementary Information is linked to the online version of the paper at
www.nature.com/nature.
Acknowledgements For logistical support, we thank K. Loftsson and the staff at Hvalur
hf; D. Ólafsdóttir, S. D. Halldórsson and G. A. Vı́kingsson at the Marine Research
Institute, Reykjavı́k; G. Bergmann and the staff at Hrefnuveiðimenn ehf; S. Raverty;
P. F. Brodie; and A. Trites. For additional samples and data, we also thank P.-Y. Daoust,
G. Williams, the Amarok Hunters and Trappers Organization of Iqaluit, Captain S. Awa
and the Inuit whaling crew from Iqaluit, J. Higgins and the Cascadia Research Collective,
M. R. Buono, A. van Helden and the Museum of New Zealand Te Papa Tongarewa, and
R. E. Fordyce. We also thank T. S. Hunter for assistance with laboratory samples.
Comments from D. J. Bohaska, M. T. Carrano, R. B. Irmis, J. G. Mead, J. F. Parham,
C. W. Potter and J. Velez-Juarbe improved this manuscript. N.D.P. was supported by a
postdoctoral research fellowship from the Natural Sciences and Engineering Research
Council of Canada and by funding from the Smithsonian Institution and its Remington
Kellogg Fund. J.A.G. was supported by a University Graduate Fellowship for Research
from the University of British Columbia, a Scripps Postdoctoral Research Fellowship
and NSERC funding to R.E.S.
Author Contributions N.D.P., J.A.G., A.W.V. and R.E.S. conducted field and laboratory
investigations and wrote the paper. G.S. provided expertise with XRCT scanning and
image reconstruction, and R.L.D. supervised the MRI reconstructions.
Author Information Reprints and permissions information is available at
www.nature.com/reprints. The authors declare no competing financial interests.
Readers are welcome to comment on the online version of this article at
www.nature.com/nature. Correspondence and requests for materials should be
addressed to N.D.P. ([email protected]).
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